Seminar given by Nick Priebe of the University of Texas at Austin to the Redwood Center for Theoretical Neuroscience at UC Berkeley on May 14, 2008.
Two views of cortical computation have been proposed to account for the selectivity of sensory neurons. In one view, excitatory afferent input provides a rough sketch of the world, which is then refined and sharpened by lateral or feedback inhibition. In the alternative view, excitatory afferent input is sufficient, on its own, to account for sensory selectivity. The debate between these perspectives has in large part been driven by the very real paradox presented by two divergent lines of evidence. On the one hand, many receptive field properties found in visual cortex, such as cross-orientation suppression and contrast-invariant orientation tuning, appear to require lateral inhibition. On the other hand, intracellular recordings have failed to find consistent evidence for lateral inhibition. I will discuss which of these two viewpoints is most appropriate to describe one feature of cortical simple cells, namely, contrast-invariant orientation tuning. A purely linear feed-forward model, incorporating only excitatory input from the thalamus, predicts that the width of orientation tuning in simple cells should broaden with contrast, breaking contrast invariance. Lateral inhibition, in the form of cross-orientation inhibition, is one mechanism that could restore contrast invariance by antagonizing feed-forward excitation at non-preferred orientations. I will demonstrate instead that the predicted broadening is suppressed by three independent mechanisms, none of which appears to require inhibition. First, many simple cells receive only some of their excitatory input from geniculate relay cells, the remainder originating from other cortical neurons with similar preferred orientations. Second, contrast-dependent changes in the trial-to-trial variability of responses lead to contrast-dependent changes in the transformation between membrane potential and spike rate. Third, membrane potential responses of simple cells saturate at lower contrasts than are predicted by a feed-forward model. Thus, the function of lateral inhibition in refining orientation selectivity is accomplished instead by a number of simple, well-defined nonlinearities of visual neurons.